Thursday, May 15, 2014

Part IV of Natural Springs, Brownback Salamanders, and the Good Folks of St. Clair County

450 million years ago northern Alabama was a shallow continental shelf accumulating thousands of feet of limey organic ooze. This layer of dead microscopic creatures eventually became solidified into thick limestone bedded between layers of sandstone, shale, and coal measures. Subsequent faulting, folding, and erosion produced the peculiar corduroy texture of the Valley and Ridge region—where pastoral valleys guarded by long parallel ridges stretch from Alabama, through the Shenandoah to Pennsylvania, and beyond. The old limestone beds typically make up the floors of the valleys—the Birmingham, Big Canoe, Shoal Creek, and Coosa Valleys, among others. Rain falling on the ridges bracketing each valley finds its way into caves, grottoes, and deep aquifers. This water gurgles out in a thousand springs.

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A male Brownback Salamander from the AppalachianPlateau of Alabama. These were identified by Mount as the "Cole Springs" form of the Two-lined Salamander. We determined they are a unique branch of the Brownback Salamander tree.

In a nutshell, we eventually confirmed that the Brownback Salamander is indeed a species separate from the Southern Two-lined Salamander. Genetically, all the spring dwellers were each other’s closest relatives, and all the stream dwellers were their own closest relatives. We also found that there were three main branches on the Brownback Salamander family tree, each of which corresponded to a region of springs with its own special spring-dwelling darter. In the Birmingham Valley there is the Watercress Darter. In the Coosa Valley there is the Coldwater Darter (Etheostoma ditrema). And in the Appalachian Plateau there are more spring-dwelling darter species.

Our genetics paper underscored the fact that the Brownback Salamander’s genetic diversity reflected the diversity of the fish in the Southern Appalachian springs. We eventually found Two-lined Salamanders right next door to nearly every spring, and they were not related to the big-headed salamanders like Folkerts predicted they would be. So why had there been so much confusion?

The phylogenetic tree we recovered based upon the DNAof the salamanders we collected; note that the spring-dwellingsalamanders we collected from the three regions are all closelyrelated to each other and not to Southern Two-lined Salamanderscollected from the same regions. Each major branch of BrownbackSalamanders correspond to unique spring-dwelling fish foundin the same springs

I think a lot of the confusion came from relying on color too much, because these and many other salamanders can change color rather rapidly. They might start out a deep brown and after two hours in a ziplock bag they turn bright

yellow. The yellow “intermediate” female we found in Shoal Creek was probably that color due to the different water temperature of the creek relative to the spring. We also found that females of the two species are not very different. But the head shape and body shape of males in the two species could not have been more different. I always use tanagers and buntings as an analogy. If you look at the males of the four North American species of these birds, there can hardly be any confusion. But try identifying the females in one of the places where their distributions overlap. By comparing the genetic features of the many salamanders we collected, we had a way to group them without any preconceived bias. We had a so-called “a priori” way to group them. When we grouped them by their genetic assignments, we found they were very different in shape. The “intermediates” we found were not genetically intermediate. They were female Brownback Salamanders.

Along with the genetic differences, we found differences in their behavior and reproductive biology. At this point (during 2009-2010) I was working with Jennifer Deitloff, a whip-smart post doc who joined the Guyer lab and shocked the Auburn scene with the progressiveness of her piercings and her utter disregard for social norms like laughing at an acceptable volume. As well, I was joined by a bright young undergraduate Mike Alcorn, who usually had poofy hair.

Rose and Bush had mentioned that the Brownback Salamander laid large numbers of eggs compared to other Eurycea. But after the long, pained taxonomic history of this salamander it was good to confirm this now that we knew what species we were dealing with. They indeed lay much larger clutches. And there was the interesting way that the males and females seemed to participate in rearing the eggs.

A female Brownback Salamander with eggs.

During the late winter of 2009 I returned to Sander’s Spring to take advantage of the potted plant nesting habitat there. I turned as many pots as possible and if there was a salamander under it I noted its sex, took a picture of the eggs, and a close up picture of the back of the salamander. Each salamander has a unique pattern of splotches and spots on the back, and I intended to use this pattern to compare to a later photo. I just wanted to confirm that the males stick around for a time instead of just hanging around with the females at the precise moment they lay the eggs. Lungless salamanders mate long before they lay their eggs and the females store the sperm. So it was quite unusual to have males anywhere near the nests.

While I prepared the study site, catching and photographing salamanders, the family patriarch came by. Buford Sanders was Al’s father. The two lived on the same old family plot but in different houses. Buford lived in the white house up the hill. Unlike Al, Buford was a very amicable old fella—always wearing overalls and an old ball cap, with worn crow’s feet at his eyes that betrayed how frequently he smiled. He was always quick with some witticism and was guaranteed to poke a little fun at Auburn’s football record or the desperate need for Mike Alcorn to get a haircut. But this was always with a terrific, twinkling smile. While I worked he came by to see what I was doing and I tried to explain to him what was unusual about what we observed, sure as always to point out how helpful it was to have such a site to return to. While I spoke he broke off a piece of watercress and munched on it.

I came back a few days later and found many of the same salamanders—including the males—were under the same pots with the same clutch of eggs. Nobody had really ever tried to confirm that the same female Eurycea stays with eggs, much less the males.

As these observations accumulated—the different genetics, habitats, head shapes, and reproductive behavior, I started thinking about what could cause all of these differences. There is a range of variation in these salamanders from big heads to skinny heads. Some species show one shape, other species show the other, and some kinds can even have both simultaneously. I thought that the habitat differences could explain this pattern; especially how the habitat could influence the distribution of females. Bird biologists discovered long ago that the distribution of females can determine the mating system of the males. If a male can monopolize several females, he will guard a territory and exploit them. If he can’t, he may choose to be monogamous.

This made sense for our salamanders: the spring habitat of Brownback Salamanders is a confined space and all the females go there to reproduce. Males could take advantage of this concentration of females. In this way, Brownback Salamanders are more like pond-breeding salamanders than other lungless salamanders. I think that’s why it’s sometimes hard to find adults: I think they migrate to the springs solely for breeding and are otherwise terrestrial. The streams and swamps occupied by Two-lined Salamanders are much more expansive than the springs. In such habitats a male would be lucky to find a single female to mate with. Perhaps in some places two kinds of males attempt both strategies simultaneously.

So I began to think the Brownback Salamander’s big head and jaw muscles were for establishing and defending territories. They were battlers. The only evidence I had at first was that occasionally males I found had bite scars, which faded after preservation. I thought the cirri of Two-lined Salamanders were for tracking females along stretches of stream habitat—cirri are known to conduct chemical cues (such as pheromones) up to the nostrils of salamanders for processing by the brain. Longer cirri, better tracking abilities. But then we tried the experiment to see if the Brownback Salamanders were territorial, when mixed with intruders both species did nothing. We were so desperate we started looking into the guts of preserved specimens of both species to see if there could be something unique about the diets of male Brownback Salamanders. Perhaps they were crunching on all those snails you find in the spring habitat. We were grasping at straws.

That’s when I decided we had not properly tested the hypothesis. If the males guard nests, and guard females from other males, then we had to check to see if they would fight in the presence of females. In early 2012 I got online to look up Al Sander’s phone number so I could call ahead, which I did every time I planned a collection trip up to Sander’s Spring.